Effects of freshwater and saltwater adaptation and dietary salt on fluid compartments, blood pressure, and venous capacitance in trout

Abstract

Olson KR, Hoagland TM. Effects of freshwater and saltwater adaptation and dietary salt on fluid compartments, blood pressure, and venous capacitance in trout. Am J Physiol Regul Integr Comp Physiol 294: R1061-R1067, 2008. First published January 9, 2008 doi:10.1152/ajpregu.00698.2007.-Trout are of interest in defining the relationship between fluid and salt balance on cardiovascular function because they thrive in freshwater (FW; volume loading, salt depleting), saltwater (SW; volume depleting, salt loading), and FW while fed a high-salt diet (FW-HS; volume and salt loading). The effects of chronic (Ͼ2 wk) adaptation to these three protocols on blood volume ( 51 Cr red cell space), extracellular fluid volume ( 99m Tc-diethylene triaminepenta-acetic acid space), arterial (dorsal aortic; PDA) and venous (ductus Cuvier; Pven) blood pressure, mean circulatory filling pressure (zero-flow Pven), and vascular capacitance were examined in the present study on unanesthetized rainbow trout. Blood volume, extracellular fluid volume, PDA, Pven, and mean circulatory filling pressure progressively increased in the order SW Ͻ FW Ͻ FW-HS. Vascular capacitance in SW fish appeared to be continuous with the capacitance curve of FW fish and reflect a passive volume-dependent unloading of the venous system of FW fish. Vascular capacitance curves for FW-HS fish were displaced upward and parallel to those of FW fish, indicative of an active increase in unstressed blood volume without any change in vascular compliance. These studies are the first in any vertebrate to measure the relationship between fluid compartments and cardiovascular function during independent manipulation of volume and salt balance, and they show that volume, but not salt, balance is the primary determinant of blood pressure in trout. They also present a new paradigm with which to investigate the relative contributions of water and salt balance in cardiovascular homeostasis. fish; unstressed blood volume; mean circulatory filling pressure; osmoregulation; ionoregulation THE PIONEERING STUDIES OF Goldblatt et al. (13), Guyton et al. (15), Dahl and Heine (8), and others clearly showed that salt and water balance were primary effectors of blood pressure in mammals. Although a direct effect of salt balance on blood pressure has been suggested (2), it is generally accepted that fluid volume is the primary effector of blood pressure and that salt balance is regulated to maintain fluid volume. This is not surprising, as water loss in the urine or through evaporation is a chronic problem for terrestrial vertebrates, and, because water is not actively transported, it can only be retained if osmotically coupled to an osmolyte, usually salt. However, the inexorable coupling of water and salt has been problematic in understanding the pathophysiology of blood pressure regulation (2, 19, 35).The relative impact of volume regulation and salt balance on blood pressure regulation in fish may be more amenable to experimentation. Saltwater (SW) fish live in an environment with a ...

The response of non-traditional natriuretic peptide production sites to salt and water manipulations in the rainbow trout

“…Supporting the hypothesis that brain NPR-B is responsive to volume status, eel NPR-B in the brain is found at lower levels in SW eels than FW eels (Katafuchi et al, 1994). Although expression of atrial CNP mRNA in FW fish is markedly lower than other cardiac NPs (Inoue et al, 2003), the significantly elevated response of atrial CNP to chronic and acute volume expansion suggests CNP as well as NPR-B (Johnson and Olson, 2009) are vital components in circumventing detrimental cardiodilation, a likely consequence of the elevated blood volume found in FW-HSD trout (Olson and Hoagland, 2008). In mammalian models, the responsiveness of the NP system in non-traditional production sites, such as ANP and BNP in the CNS, has been well demonstrated.…”

“…Based on the limited available studies, this seems to indeed be the case (Chen et al, 2007;Olson and Hoagland, 2008;Perry et al, 2006). The adaptation from FW to SW results in a significantly elevated plasma osmolarity, and has been reported to produce a significantly lower dorsal aortic pressure (P DA ), central venous pressure (P VEN ) and mean circulatory filling pressure (MCFP) largely via a reduction in blood volume.…”

“…A limited amount of de-ionized water was added to this mixture and the paste was then squeezed through a potato ricer and dried at room temperature overnight. This HSD feeding regime has been shown to increase gill chloride cell numbers and Na + /K + -ATPase activity, dorsal aortic (DA) pressure, central venous pressure and blood volume in FW rainbow trout (Chen et al, 2007;Olson and Hoagland, 2008;Salman and Eddy, 1987).…”

Endogenous vascular synthesis of B-type and C-type natriuretic peptides in the rainbow trout

“…It can be reasonably proposed that preload and cardiac filling pressure are likely even more important for determining V S in fish than in mammals, as the ejection fraction for fish hearts is quite high (80-100%) (Sandblom and Axelsson, 2007). Thus, it is likely that active regulation of venous tone is especially vital in euryhaline fishes that experience a wide range of osmotic stresses and subsequent perturbations in blood volume (Olson and Hoagland, 2008).…”

“…Vascular capacitance curves were constructed from measurements on conscious trout in vivo using the ventral aorta occlusion method to establish zero-flow cardiac output as previously described (Olson and Hoagland, 2008;Zhang et al, 1998). Briefly, P DA and P VEN were measured in unanesthetized fish before and during occlusion of the ventral aorta.…”